Adding up the odds-Nitric oxide signaling underlies the decision to flee and post-conflict depression of aggression.

Stevenson PA, Rillich J - Sci Adv (2015)

Bottom Line:
We found that crickets, which exhibit spectacular fighting behavior, flee once the sum of their opponent's aversive actions accrued during fighting exceeds a critical amount.This effect of aversive experience is mediated by the NO signaling pathway.NO's effect is manifested in losers by prolonged avoidance behavior, characteristic for social defeat in numerous species.

ABSTRACTFighting is dangerous, which is why animals choose to flee once the costs outweigh the benefits, but the mechanisms underlying this decision-making process are unknown. By manipulating aggressive signaling and applying nitrergic drugs, we show that the evolutionarily conserved neuromodulator nitric oxide (NO), which has a suppressing effect on aggression in mammals, can play a decisive role. We found that crickets, which exhibit spectacular fighting behavior, flee once the sum of their opponent's aversive actions accrued during fighting exceeds a critical amount. This effect of aversive experience is mediated by the NO signaling pathway. Rather than suppressing aggressive motivation, NO increases susceptibility to aversive stimuli and with it the likelihood to flee. NO's effect is manifested in losers by prolonged avoidance behavior, characteristic for social defeat in numerous species. Intriguingly, fighting experience also induces, via NO, a brief susceptible period to aversive stimuli in winners just after victory. Our findings thus reveal a key role for NO in the mechanism underlying the decision to flee and post-conflict depression in aggressive behavior.

Mentions:
To test our hypothesis that crickets summate information from their opponent’s actions during fighting for the decision to flee (12), we investigated how winners respond to new opponents at various times after victory. As in many species (18), crickets that win are typically highly aggressive (23) and, when matched 3 or 10 min after victory, fought ferociously and won practically half the contests against standard hyper-aggressive opponents (Fig. 4; data for 10 min: median level 6, IQR 5 to 6, median duration 18 s, IQR 10 to 29, win chance: 47%, n = 17). However, when fights were staged immediately after victory, the winners were far less aggressive (U tests versus 10 min: Plevel = 0.0049, Pduration = 0.0014), and they mostly retreated from hyper-aggressive opponents (16% wins, n = 19, χ2 compared to 50%: 4.97, P = 0.026). This suggests that freshly established winners still bear a short-term record of their previous opponent’s (the loser’s) agonistic actions. Supporting this, and the notion that opponent actions activate the NO signaling pathway, the brief susceptible period when winners are more likely to lose was not evident in LNAME-treated winners (median level 6, IQR 4.75 to 6, median duration 17 s, IQR 7 to 22, win chance: 42%, n = 26, U tests versus DNAME: Plevel = 0.0077, Pduration = 0.0068; Fig. 4). Blocking NO does not lead to a general increase in the tendency of winners to fight and win, because LNAME failed to increase the level and duration of fights or win chances against hyper-aggressive opponents when staged 3 or 10 min after the susceptible period.

Mentions:
To test our hypothesis that crickets summate information from their opponent’s actions during fighting for the decision to flee (12), we investigated how winners respond to new opponents at various times after victory. As in many species (18), crickets that win are typically highly aggressive (23) and, when matched 3 or 10 min after victory, fought ferociously and won practically half the contests against standard hyper-aggressive opponents (Fig. 4; data for 10 min: median level 6, IQR 5 to 6, median duration 18 s, IQR 10 to 29, win chance: 47%, n = 17). However, when fights were staged immediately after victory, the winners were far less aggressive (U tests versus 10 min: Plevel = 0.0049, Pduration = 0.0014), and they mostly retreated from hyper-aggressive opponents (16% wins, n = 19, χ2 compared to 50%: 4.97, P = 0.026). This suggests that freshly established winners still bear a short-term record of their previous opponent’s (the loser’s) agonistic actions. Supporting this, and the notion that opponent actions activate the NO signaling pathway, the brief susceptible period when winners are more likely to lose was not evident in LNAME-treated winners (median level 6, IQR 4.75 to 6, median duration 17 s, IQR 7 to 22, win chance: 42%, n = 26, U tests versus DNAME: Plevel = 0.0077, Pduration = 0.0068; Fig. 4). Blocking NO does not lead to a general increase in the tendency of winners to fight and win, because LNAME failed to increase the level and duration of fights or win chances against hyper-aggressive opponents when staged 3 or 10 min after the susceptible period.

Bottom Line:
We found that crickets, which exhibit spectacular fighting behavior, flee once the sum of their opponent's aversive actions accrued during fighting exceeds a critical amount.This effect of aversive experience is mediated by the NO signaling pathway.NO's effect is manifested in losers by prolonged avoidance behavior, characteristic for social defeat in numerous species.

ABSTRACTFighting is dangerous, which is why animals choose to flee once the costs outweigh the benefits, but the mechanisms underlying this decision-making process are unknown. By manipulating aggressive signaling and applying nitrergic drugs, we show that the evolutionarily conserved neuromodulator nitric oxide (NO), which has a suppressing effect on aggression in mammals, can play a decisive role. We found that crickets, which exhibit spectacular fighting behavior, flee once the sum of their opponent's aversive actions accrued during fighting exceeds a critical amount. This effect of aversive experience is mediated by the NO signaling pathway. Rather than suppressing aggressive motivation, NO increases susceptibility to aversive stimuli and with it the likelihood to flee. NO's effect is manifested in losers by prolonged avoidance behavior, characteristic for social defeat in numerous species. Intriguingly, fighting experience also induces, via NO, a brief susceptible period to aversive stimuli in winners just after victory. Our findings thus reveal a key role for NO in the mechanism underlying the decision to flee and post-conflict depression in aggressive behavior.